Flying insects have the highest mass-specific metabolic rate of all animals. Oxygen is supplied to the flight muscles by a combination of diffusion and convection along the internal air-filled tubes of the tracheal system. This study measured maximum flight metabolic rate (FMR) during tethered flight in the migratory locust Locusta migratoria under varying oxygen partial pressure (PO₂ ) in background gas mixtures of nitrogen (N₂), sulfur hexafluoride (SF₆) and helium (He), to vary O₂ diffusivity and gas mixture density independently. With N₂ as the sole background gas (normodiffusive-normodense), mass-independent FMR averaged 132±19 mW g⁻⁰·⁷⁵ at normoxia (PO₂ =21 kPa), and was not limited by tracheal system conductance, because FMR did not increase in hyperoxia. However, FMR declined immediately with hypoxia, oxy-conforming nearly completely. Thus, the locust respiratory system is matched to maximum functional requirements, with little reserve capacity. With SF₆ as the sole background gas (hypodiffusive-hyperdense), the shape of the relationship between FMR and PO₂ was similar to that in N₂, except that FMR was generally lower (e.g. 24% lower at normoxia). This appeared to be due to increased density of the gas mixture rather than decreased O₂ diffusivity, because hyperoxia did not reverse it. Normoxic FMR was not significantly different in He-SF₆ (hyperdiffusive-normodense) compared with the N₂ background gas, and likewise there was no significant difference between FMR in SF₆-He (normodiffusive-hyperdense) compared with the SF₆ background gas. The results indicate that convection, not diffusion, is the main mechanism of O₂ delivery to the flight muscle of the locust when demand is high.